Abstract
ABSTRACT An outstanding challenge in developmental biology is to reveal the mechanisms underlying the morphogenesis of complex organs. A striking example is the developing inner ear of the vertebrate, which acquires a precise three-dimensional arrangement of its constituent epithelial cells to form three semicircular canals, a central vestibule and a coiled cochlea (in mammals). In generating a semicircular canal, epithelial cells seem to ‘disappear’ from the center of each canal. This phenomenon has been variously explained as (i) transdifferentiation of epithelium into mesenchyme, (ii) absorption of cells into the expanding canal or (iii) programmed cell death. In this study, an in situ DNA-end labeling technique (the TUNEL protocol) was used to map regions of cell death during inner ear morphogenesis in the chicken embryo from embryonic days 3.5-10. Regions of cell death previously identified in vertebrate ears have been confirmed, including the ventromedial otic vesicle, the base of the endolymphatic duct and the fusion plates of the semicircular canals. New regions of cell death are also described in and around the sensory organs. Reducing normal death using retrovirus-mediated overexpression of human bcl-2 causes abnormalities in ear morphogenesis: hollowing of the center of each canal is either delayed or fails entirely. These data provide new evidence to explain the role of cell death in morphogenesis of the semicircular canals.
References
37
Referenced
109
10.1002/ar.1092280311
/ Anat. Rec / Shaping, invagination, and closure of the chick embryo otic vesicle: Scanning electron microscope and quantitative study by Alvarez (1990)10.1002/cne.903140410
/ J. Comp. Neurol / Appearance and distribution of the 275kD hair-cell antigen during development of the inner ear by Bartolami (1991)10.1002/(SICI)1096-9861(19960513)368:4<620::AID-CNE12>3.0.CO;2-L
/ J. Comp. Neurol / Standard atlas of the gross anatomy of the developing inner ear of the chicken by Bissonnette (1996)10.1242/dev.114.2.379
/ Development / The fate of medial edge epithelial cells during palatal fusion in vitro: An analysis by DiI labeling and confocal microscopy by Carrette (1992)10.1007/BF00174615
/ Anat. Embryol / Developmental cell death: morphological diversity and multiple mechanisms by Clarke (1990)10.1016/0166-2236(95)93928-Q
/ Trends in Neuroscience / The Bcl-2 family of proteins, and the regulation of neuronal survival by Davies (1995)10.1159/000147752
/ Acta. Anat / Epithelium-mesenchyme transition during neural crest development by Duband (1995){'key': '2025021403435397900_DEVELOP_124_12_2451C8', 'first-page': '2604', 'article-title': 'Replication-competent retroviral vectors encoding alkaline phosphatase reveal spatial restriction of viral gene expression/transduction in the chick embryo', 'volume': '13', 'author': 'Fekete', 'year': '1993', 'journal-title': 'Mol. Cell. Biol'}
/ Mol. Cell. Biol / Replication-competent retroviral vectors encoding alkaline phosphatase reveal spatial restriction of viral gene expression/transduction in the chick embryo by Fekete (1993)10.1242/dev.103.Supplement.41
/ Development / Palate development by Ferguson (1988)10.1016/S0012-1606(89)80017-X
/ Dev. Biol / Medial edge epithelium transforms to mesenchyme after embryonic palatal shelves fuse by Fichett (1989){'key': '2025021403435397900_DEVELOP_124_12_2451C11', 'article-title': 'Early embryology of the vertebrate ear', 'volume-title': 'In Development of the Auditory System', 'author': 'Fritzsch', 'year': '1997'}
/ In Development of the Auditory System / Early embryology of the vertebrate ear by Fritzsch (1997)10.1242/dev.122.8.2349
/ Development / Role of TGFs and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod by Ganan (1996)10.1083/jcb.119.3.493
/ J. Cell Biol / Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation by Gavrieli (1992){'key': '2025021403435397900_DEVELOP_124_12_2451C14', 'first-page': '419', 'article-title': 'Bcl-2 expressed using a retroviral vector is localized primarily in the nuclear membrane and the endoplasmic reticulum of chicken embryo fibroblasts', 'volume': '5', 'author': 'Givol', 'year': '1994', 'journal-title': 'Cell Growth Differ'}
/ Cell Growth Differ / Bcl-2 expressed using a retroviral vector is localized primarily in the nuclear membrane and the endoplasmic reticulum of chicken embryo fibroblasts by Givol (1994)10.1111/j.1469-185X.1951.tb00774.x
/ Biological Review / Cell deaths in normal vertebrate ontogeny by Glucksmann (1951)10.1242/dev.116.4.1087
/ Development / Epithelial-mesenchymal transformation during palatal fusion: carboxyflourescein traces cells at light and electron microscopic levels by Griffith (1992)10.1242/dev.112.2.541
/ Development / Hyaluronan as a propellant for epithelial movement: the development of semicircular canals in the inner ear of Xenopus by Haddon (1991)10.1002/(SICI)1096-9861(19960129)365:1<113::AID-CNE9>3.0.CO;2-6
/ J. Comp. Neurol / Early ear development in the embryo of the zebrafish, Danio rerio by Haddon (1996)10.1002/jmor.1050880104
/ J. Morph / A series of normal stages in the development of the chick embryo by Hamburger (1951)10.1242/jcs.8.1.229
/ J. Cell Sci / Tetrazolium salt and electron-microscopic studies of cellular degeneration and necrosis in the interdigital areas of the developing chick limb by Hammar (1971)10.1242/dev.120.8.2121
/ Development / Expression of baculovirus P35 prevents cell death in Drosophila by Hay (1994)10.1002/(SICI)1097-0177(199605)206:1<112::AID-AJA10>3.0.CO;2-7
/ Dev. Dynamics / High efficiency gene transfer into the embryonic chicken CNS using B-subgroup retroviruses by Homburger (1996)10.1159/000259226
/ Audiology and Neuro-Otology / In vivo gene transfer into the embryonic inner ear using retroviral vectors by Kiernan (1997)10.1002/jmor.1051210302
/ J. Morph / Correlation of the development of membranous and bony labyrinths, acoustic ganglia, nerves, and brain centers in the chick embryo by Knowlton (1967)10.1288/00005537-197609000-00015
/ Laryngoscope / The role of cellular degeneration in the normal development of (rat) otocyst by Marovitz (1976)10.1177/00034894770860S102
/ Annals of Otology, Rhinology and Laryngology / Ultrastructural development of the early rat otocyst by Marovitz (1977)10.1006/dbio.1993.1263
/ Dev. Biol / Descriptive and experimental analysis of the epithelial remodellings that control semicircular canal formation in the developing mouse inner ear by Martin (1993)10.1016/S0091-679X(08)60629-9
/ In Methods in Avian Embryology / Manipulating gene expression with replication competent retroviruses by Morgan (1996)10.1083/jcb.124.1.1
/ J. Cell Biol / Bcl-2 and the regulation of programmed cell death by Reed (1994)10.1177/000348949009900613
/ Annals of Otology, Rhinology and Laryngology / Patterns of epithelial cell death during early development of the human inner ear by Represa (1990){'key': '2025021403435397900_DEVELOP_124_12_2451C31', 'first-page': '131', 'article-title': 'Programmed cell death is involved in chicken ear development', 'volume': '522', 'author': 'Riedl', 'year': '1997', 'journal-title': 'Assoc. Res. Otolaryngol. Abs'}
/ Assoc. Res. Otolaryngol. Abs / Programmed cell death is involved in chicken ear development by Riedl (1997)10.1007/BF00363214
/ Roux’s Arch. Dev. Biol / Neurulation in the anterior trunk region of the zebrafish Brachydanio rerio by Schmitz (1993)10.1016/0012-1606(92)90071-N
/ Dev. Biol / Medial edge epithelium fate traced by cell lineage analysis during epithelial-mesenchymal transformation in vivo by Schuler (1992)10.1242/dev.120.9.2601
/ Development / Programmed cell death is affected in the novel mouse mutant Fused toes (Ft) by van der Hoeven (1994)10.1002/ar.1092100113
/ Anat. Rec / Epithelial fusion during early semicircular canal formation in the embryonic zebrafish, Brachydanio rerio by Waterman (1984)10.1242/dev.122.12.3725
/ Development / BMP-2/-4 mediate programmed cell death in chicken limb buds by Yokouchi (1996)10.1126/science.272.5262.738
/ Science / Requirement for BMP signaling in interdigital apoptosis and scale formation by Zou (1996)
Dates
Type | When |
---|---|
Created | 4 years, 4 months ago (April 23, 2021, 3:13 p.m.) |
Deposited | 6 months, 3 weeks ago (Feb. 13, 2025, 10:44 p.m.) |
Indexed | 1 month, 3 weeks ago (July 16, 2025, 8:06 a.m.) |
Issued | 28 years, 2 months ago (June 15, 1997) |
Published | 28 years, 2 months ago (June 15, 1997) |
Published Online | 28 years, 2 months ago (June 15, 1997) |
Published Print | 28 years, 2 months ago (June 15, 1997) |
@article{Fekete_1997, title={Involvement of programmed cell death in morphogenesis of the vertebrate inner ear}, volume={124}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.124.12.2451}, DOI={10.1242/dev.124.12.2451}, number={12}, journal={Development}, publisher={The Company of Biologists}, author={Fekete, Donna M. and Homburger, Sheila A. and Waring, Michael T. and Riedl, Ann E. and Garcia, Luis F.}, year={1997}, month=jun, pages={2451–2461} }